Young and mature leaves of three Acer truncatum varieties with different leaf colors were examined. Transcriptome sequencing and flavonoid metabolism were used to analyze the differential gene expression associated with different leaf colors and growth stages and the relationships between gene expression and flavonoid and anthocyanin contents to improve ornamental value and develop flavonoid-rich A. truncatum. Kyoto Encyclopedia of Genes and Genomes database annotation of differentially expressed genes indicated that the following genes were related to flavonoid synthesis: phenylpropanoid biosynthesis genes (PAL, C4H, 4CL and CHS), flavonoid biosynthesis genes (E2.1.1.104, CHI, FLS, F3′5′H and ANR), anthocyanin biosynthesis genes (ANS, DFR, HCT, BZ1, GT1, and UGT79B1), isoflavonoid biosynthesis genes (HIDH and CYP81E17), and their transcriptional regulator (MYB). A total of 234 types of flavonoids were detected. The types and contents of anthocyanins in the red-leaf varieties ‘Hong Jingling’ and ‘Caidie Fanfei’ were significantly higher than those in the green leaf cultivar ‘Lv Baoshi’, especially morning glory 3-O-glucoside, delphinidin 3-O-glucoside, and pelargonium-3-O-glucoside, which were not detected in 'Lv Baoshi'. Combined omics analysis showed that downregulated expression of C4H, CHS and F3′5′H and upregulated expression of FLS reduced the supply of raw materials for anthocyanin synthesis, and downstream ANR upregulation converted anthocyanins to procyanidins, increasing the total flavonoid content. F3′5′H expression was downregulated in the leaves of each variety with development, resulting in the accumulation of catechins and the gradual greening of the leaves. F3′5′H was significantly depleted in the young leaves of ‘Hong Jingling’ and ‘Caidie Fanfei’ compared with the young leaves of ‘Lv Baoshi’, while ANS and BZ1 were enriched significantly. It is concluded that F3′5′H, BZ1, and ANS are the key genes needed for breeding red A. truncatum and that ANR is the key gene needed for breeding varieties with a high flavonoids contens. These results may facilitate genetic modification or selection for further improvement of the ornamental qualities and flavonoid content of A. truncatum.
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